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Cerebral representation of vocalization in the squirrel monkey

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Summary

Specific vocalization types following electrical stimulation of 5940 electrode positions are studied in 39 squirrel monkeys. Except cerebellum, caudal medulla, and a few cortical areas, the sites of stimulation were distributed throughout the brain. Each vocalization elicited was tested for reproducibility at the site of stimulation and in homologue structures. All vocalizations were analyzed spectrographically and then classified for eight fundamental vocalization types.

The cerebral distribution of two call types forms continuous systems extending from midbrain via diencephalon into forebrain; the remaining call types are represented in several separate areas not continuous with each other. In medulla and pons the responsive substrates for vocalization follow the course of the spinothalamic tract; in midbrain they lie within the periaqueductal gray, lateral tegmentum, and lemniscus medialis; in diencephalon they are found in the hypothalamus and midline thalamus; in forebrain, finally they are distributed over amygdala, stria terminalis, substantia innominata, preoptic region, septum, rostral hippocampus, posteromedial orbital cortex, cingulate gyrus, and rostroventral temporal cortex. Hence a close relation between limbic system and vocalization producing substrates emerges.

Among the brain structures yielding vocalization the mesencephalic periaqueductal gray is assumed to be the region where the electrical stimulus interferes most directly with specific vocalization mechanisms.

Besides the anatomical site of stimulation the set of stimulus parameters is important for the elicitation of vocalizations. Relations between amplitude, frequency, and duration of impulses on the one hand and type, loudness, rhythm, duration, and latency of vocalization on the other hand were tested. The influence of the stimulus set on the reaction parameters depends also on the relative position of the electrode within the effective structure. Proper manipulation of stimulus parameters often results in the disintegration of a complex stimulus response into single components.

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Abbreviations

a:

Nucl. accumbens

aa:

Area anterior amygdalae

ab:

Nucl. basalis amygdalae

ac:

Nucl. centralis amygdalae

al:

Nucl. lateralis amygdalae

am:

Nucl. medialis amygdalae

an:

Nucl. anterior thalami

anl:

Ansa lenticularis

aq:

Substantia grisea centralis

bc:

Brachium conjunctivum

ca:

Caudatum

cc:

Corpus callosum

cen:

Nucl. centralis superior (Bechterew)

cent:

Centrum medianum

ci:

Capsula interna

cin:

Cingulum

cl:

Claustrum

coa:

Commissura anterior

coli:

Colliculus inferior

cols:

Colliculus superior

cr:

Corpus restiforme

csp:

Tr. corticospinalis

db:

Fasc. diagonalis Brocae

dbc:

Decussatio brachii conjunctivi

f:

Fornix

gc:

Gyrus cinguli

gl:

Corpus geniculatum laterale

gm:

Corpus geniculatum mediale

gr:

Gyrus rectus

gs:

Gyrus subcallosus

h:

Campus Foreli

ha:

Nucl. habenularis

hi:

Tr. habenulointerpeduncularis

hip:

Hippocampus

hya:

Area hypothalamica anterior

hyp:

Area hypothalamica posterior

hyv:

Area hypothalamica ventralis

in:

Nucl. interpeduncularis

lap:

Nucl. lateralis posterior thalami

lav:

Nucl. lateralis ventralis thalami

le:

Lemniscus lateralis

lem:

Lemniscus medialis

lm:

Fasc. longitudinalis medialis

m:

Corpus mamillare

md:

Nucl. medialis dorsalis thalami

mt:

Tr mamillothalamicus

nst:

Nucl. striae terminalis

oi:

Nucl. olivaris inferior

ol:

Fasc. olfactorius (Zuckerkandl)

os:

Nucl. olivaris superior

p:

Pedunculus cerebri

pmc:

Brachium pontis

po:

Griseum pontis

pp:

Nucl. praepositus hypoglossi

pro:

Area praeoptica

pu:

Nucl. pulvinaris thalami

put:

Putamen

re:

Formatio reticularis tegmenti

rep:

Nucl. reticularis tegmenti pontis

rl:

Nucl. reticularis lateralis myelencephali

rub:

Nucl. ruber

s:

Septum

sm:

Stria medullaris

sn:

Substantia nigra

st:

Stria terminalis

sto:

Stria olfactoria lateralis

tec:

Tr. tegmentalis centralis

trz:

Corpus trapezoides

va:

Nucl. ventralis anterior

vpl:

Nucl. ventralis posterolaterali thalami

vpm:

Nucl. ventralis posteromedialis thalami

zi:

Zona incerta

II:

Tr. options

IICh:

Chiasma nervorum opticorum

III:

N. oculomotorius Nucl. nervi oculomotorii

IV:

N. and Nucl. nervi trochlearis

VI:

N. abducens

VII:

N. facialis

VIII:

N. acusticus

IX:

N. glossopharyngeus

References

  • Adametz, J., O'Leary, J.L.: Experimental mutism resulting from periaqueductal lesions in cats. Neurology 9, 636–642 (1959).

    Google Scholar 

  • Ban, T.: The septo-preoptico-hypothalamic system and its autonomic function. In: Progress in Brain Research, Vol. 21A. Amsterdam-London-New York: Elsevier Publ. Co. 1966.

    Google Scholar 

  • Barenne, D.J.G. de, Garol, H.W., McCulloch, W.S.: The motor cortex of the chimpanzee. J. Neurophysiol. 4, 287–303 (1941).

    Google Scholar 

  • Berry, C.M., Karl, R.C., Hinsey, J.C.: Course of spinothalamic and medial lemniscus pathways in the cat and rhesus monkey. J. Neurophysiol. 13, 149–156 (1950).

    Google Scholar 

  • Brickner, R.M.: A human cortical area producing repetitive phenomena when stimulated. J. Neurophysiol. 3, 128–130 (1940).

    Google Scholar 

  • Brown, T.G.: Note on physiology of basal ganglia and midbrain of anthropoid ape especially in reference to act of laughter. J. Physiol. (Lond.) 49, 195–207 (1915).

    Google Scholar 

  • Clark, G., Chow, K.L., Gillaspy, C.C., Klotz, D.A.: Stimulation of anterior limbic region in dogs. J. Neurophysiol. 12, 459–463 (1949).

    Google Scholar 

  • Clark, W.E.L., Boggon, B.R.: On the connections of the anterior nucleus of the thalamus. J. Anat. (Lond.) 67, 215–226 (1933).

    Google Scholar 

  • Crosby, E.C., Woodburne, R.T.: The mammalian midbrain and isthmus regions. Part II. The fiber connections. C. The hypothalamo-tegmental pathways. J. comp. Neurol. 94, 1–32 (1951).

    Google Scholar 

  • Delgado, J.M.R.: Cerebral structures involved in transmission and elaboration of noxious stimulation. J. Neurophysiol. 18, 261–275 (1955).

    Google Scholar 

  • Dua, S., MacLean, P.D.: Localization for penile erection in medial frontal lobe. Amer. J. Physiol. 207, 1425 (1964).

    Google Scholar 

  • Emmers, R., Akert, K.: A stereotaxic atlas of the brain of the squirrel monkey (Saimiri sciureus). Madison: University of Wisconsin Press 1963.

    Google Scholar 

  • Forman, D., Ward, J.W.: Responses to electrical stimulation of caudate nucleus in cats in chronic experiments. J. Neurophysiol. 20, 230–244 (1957).

    Google Scholar 

  • Fox, C.A.: Certain basal telencephalic centers in the cat. J. comp. Neurol. 72, 1–62 (1940).

    Google Scholar 

  • —: The stria terminalis, longitudinal association bundle and precommissural fornix fibers in the cat. J. comp. Neurol. 79, 277–295 (1943).

    Google Scholar 

  • Gergen, J.A., MacLean, P.D.: A stereotaxic atlas of the squirrel monkey's brain (Saimiri sciureus). Publ. Health Service Publ. No. 933, Bethesda (1962).

  • Gibbs, E.L., Gibbs, F.A.: A purring centre in the cat's brain. J. comp. Neurol. 64, 209–211 (1936).

    Google Scholar 

  • Green, H.D., Walker, A.E.: The effects of ablation of the cortical motor face area in monkeys. J. Neurophysiol. 1, 262–280 (1938).

    Google Scholar 

  • Guillery, R.W.: Degeneration in the hypothalamic connections of the albino rat. J. Anat. (Lond.) 91, 91–115 (1957).

    Google Scholar 

  • —: Afferent fibers to the dorso-medial thalamic nucleus in the cat. J. Anat. (Lond.) 93, 403–419 (1959).

    Google Scholar 

  • Hast, M.H., Milojevic, B.: The response of the vocal folds to electrical stimulation of the inferior frontal cortex of the squirrel monkey. Acta oto-laryng. (Stockh.) 61, 196–204 (1966).

    Google Scholar 

  • Hess, W.R., Brügger, M.: Das subkortikale Zentrum der affektiven Abwehrreaktion. Helv. physiol. pharmacol. Acta 1, 33–52 (1943).

    Google Scholar 

  • Hilton, S.M., Zbrozyna, A.W.: Amygdaloid region for defence reactions and its efferent pathway to the brain stem. J. Physiol. (Lond.) 165, 160–173 (1963).

    Google Scholar 

  • Hines, M.: Movements elicited from precentral gyrus of adult chimpanzees by stimulation with sine wave currents. J. Neurophysiol. 3, 442–466 (1940).

    Google Scholar 

  • Holst, E. v., Saint Paul, U. v.: Vom Wirkungsgefüge der Triebe. Naturwissenschaften 47, 409–422 (1960).

    Google Scholar 

  • Hughes, J.R., Mazurowski, J.A.: Studies on the supracallosal mesial cortex of unanesthetized, conscious mammals. II. Monkey. A. Movements elicited by electrical stimulations. Electroenceph. clin. Neurophysiol. 14, 477–485 (1962).

    Google Scholar 

  • Hunsperger, R.W.: Affektreaktionen auf elektrische Reizung im Hirnstamm der Katze. Helv. physiol. pharmacol. Acta 14, 70–92 (1956).

    Google Scholar 

  • —, Gwóždž, B.: Lokalisation zentralnervöser Strukturen für Miauen auf Grund von Hirnreizversuchen. Verh. Schweiz. Naturforsch. Ges. Zürich, pp. 228–238 (1964).

    Google Scholar 

  • Ingram, W.R., Ranson, S.W., Hannett, F.I., Zeiss, F.R., Terwilliger, E.H.: Results of stimulation of the tegmentum with the Horsley-Clarke stereotaxic apparatus. Arch. Neurol. Psychiat. (Chic.) 28, 513–541 (1932).

    Google Scholar 

  • Johnson, T.N., Rosvold, H.E., Mishkin, M.: Projections from behaviorally-defined sectors of the prefrontal cortex to the basal ganglia, septum, and diencephalon of the monkey. Exp. Neurol. 21, 20–34 (1968).

    Google Scholar 

  • Jürgens, U., Maurus, M., Ploog, D., Winter, P.: Vocalization in the squirrel monkey (Saimiri sciureus) elicited by brain stimulation. Exp. Brain Res. 4, 114–117 (1967).

    Google Scholar 

  • Kaada, B.R.: Somato-motor, autonomic and electrocorticographic responses to electrical stimulation of “rhinencephalic” and other structures in primates, cat and dog. Acta physiol. scand. Suppl. 83, 1–285 (1951).

    Google Scholar 

  • Kabat, H.: Electrical stimulation of points in the forebrain and midbrain. The resultant alterations in respiration. J. comp. Neurol. 64, 187–208 (1936).

    Google Scholar 

  • Kanai, T., Wang, S.C.: Localization of the central vocalization mechanism in the brainstem of the cat. Exp. Neurol. 6, 426–434 (1962).

    Google Scholar 

  • Kelly, A.H., Beaton, L.E., Magoun, H.W.: A midbrain mechanism for facio-vocal activity. J. Neurophysiol. 9, 181–189 (1946).

    Google Scholar 

  • Leyton, A.S.F., Sherrington, C.S.: Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Quart. J. exp. Physiol. 11, 135–222 (1917).

    Google Scholar 

  • Loo, Y.T.: The forebrain of the opossum, Didelphis virginiana. Part II. Histology. J. comp. Neurol. 52, 1–148 (1931).

    Google Scholar 

  • MacLean, P.D.: Chemical and electrical stimulation of hippocampus in unrestrained animals. Arch. Neurol. Psychiat. (Chic.) 78, 113–142 (1957).

    Google Scholar 

  • —, Delgado, J.M.R.: Electrical and chemical stimulation of frontotemporal portion of limbic system in the waking animal. Electroenceph. clin. Neurophysiol. 5, 91–100 (1953).

    Google Scholar 

  • —, Denniston, R.H., Dua, S.: Further studies on cerebral representation of penile erection: caudal thalamus, midbrain, pons. J. Neurophysiol. 26, 273–293 (1963).

    Google Scholar 

  • Magoun, H.W., Atlas, D., Ingersoll, E.H., Ranson, S.W.: Associated facial, vocal and respiratory components of emotional expression. An experimental study. J. Neurol. Psychopath. 17, 241–255 (1937).

    Google Scholar 

  • Maurus, M., Mitra, J., Ploog, D.: Cerebral representation of the clitoris in ovariectomized squirrel monkeys. Exp. Neurol. 13, 283–288 (1965).

    Google Scholar 

  • Mehler, W.R., Feferman, M.E., Nauta, W.J.H.: Ascending axon degeneration following anterolateral chordotomy. An experimental study in the monkey. Brain 83, 718–750 (1960).

    Google Scholar 

  • Meyer, A.E., Hess, W.R.: Diencephal ausgelöstes Sexualverhalten und Schmeicheln bei der Katze. Helv. physiol. pharmacol. Acta 15, 401–407 (1957).

    Google Scholar 

  • Molina, A.P. de, Hunsperger, R.W.: Organization of the subcortical system governing defence and flight reactions in the cat. J. Physiol. (Lond.) 160, 200–213 (1962).

    Google Scholar 

  • Nauta, W.J.H.: Hippocampal projections and related neural pathways to the midbrain in the cat. Brain 81, 319–340 (1958).

    Google Scholar 

  • —: Neural associations of the amygdaloid complex in the monkey. Brain 85, 505–520 (1962).

    Google Scholar 

  • —, Kuypers, H.G.J.M.: Some ascending pathways in the brain stem reticular formation. In: Reticular formation of the brain. Ed. by H. Jasper et al. Boston: Little, Brown 1958.

    Google Scholar 

  • —, Whitlock, D.G.: An anatomical analysis of the non-specific thalamic projection system. In: Brain mechanisms and consciousness. Ed. by J.F. Delafresnaye. Oxford: Blackwell 1954.

    Google Scholar 

  • Penfield, W., Roberts, L.: Speech and brain mechanisms. Princeton: Princeton University Press 1959.

    Google Scholar 

  • —, Welch, K.: The supplementary motor area of the cerebral cortex. Arch. Neurol. Psychiat. (Chic.) 66, 289–317 (1951).

    Google Scholar 

  • Phillips, R.E.: Electrically elicited vocalizations in chickens and Mallard ducks. 10th Int. Ethological Conference, Stockholm 1967.

  • Powell, E.W.: Septal efferents in the cat. Exp. Neurol. 14, 328–337 (1966).

    Google Scholar 

  • Powell, T.P.S., Cowan, W.M.: A study of thalamo-striate relations in the monkey. Brain 79, 364–390 (1956).

    Google Scholar 

  • Raisman, G., Cowan, W.M., Powell, T.P.S.: An experimental analysis of the efferent projection of the hippocampus. Brain 89, 83–108 (1966).

    Google Scholar 

  • Robinson, B.W.: Vocalization evoked from forebrain in Macaca mulatta. Physiol. Behav. 2, 345–354 (1967).

    Google Scholar 

  • Rosabal, F.: Cytoarchitecture of the frontal lobe of the squirrel monkey. J. comp. Neurol. 130, 87–108 (1967).

    Google Scholar 

  • Rose, J.E., Woolsey, C.N.: Structures and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat. J. comp. Neurol. 89, 279–347 (1948).

    Google Scholar 

  • Scheibel, M.E., Scheibel, A.B.: Structural organization of non-specific thalamic nuclei and their projection toward cortex. Brain Res. 6, 60–94 (1967).

    Google Scholar 

  • Schmidt, R.S.: Central mechanisms of frog calling. Behaviour 26, 251–285 (1966).

    Google Scholar 

  • Showers, M.J.C., Crosby, E.C.: Somatic and visceral responses from the cingulate gyrus. Neurology 8, 561–565 (1958).

    Google Scholar 

  • Skultety, F.M.: Experimental mutism in dogs. Arch. Neurol. (Chic.) 6, 235–241 (1962).

    Google Scholar 

  • —: Stimulation of periaqueductal gray and hypothalamus. Arch. Neurol. (Chic.) 8, 608–620 (1963).

    Google Scholar 

  • —: Mutism in cats with rostral midbrain lesions. Arch. Neurol. (Chic.) 12, 211–225 (1965).

    Google Scholar 

  • Sloan, N., Kaada, B.R.: Effects of anterior limbic stimulation on somato-motor and electrocortical activity. J. Neurophysiol. 16, 203–220 (1953).

    Google Scholar 

  • Smith, W.K.: The functional significance of the rostral cingular cortex as revealed by its responses to electrical excitation. J. Neurophysiol. 8, 241–255 (1945).

    Google Scholar 

  • —: The results of stimulation of the uncus and adjacent portions of the hippocampal gyrus. Fed. Proc. 3, 43 (1944).

    Google Scholar 

  • Spiegel, E.A., Kletzkin, M., Szekeley, E.G.: Pain reactions upon stimulation of the tectum mesencephali. J. Neuropath. exp. Neurol. 13, 212–220 (1954).

    Google Scholar 

  • Sugar, O., Chusid, J.G., French, J.D.: A second motor cortex in the monkey (Macaca mulatta). J. Neuropath. exp. Neurol. 7, 182–189 (1948).

    Google Scholar 

  • Valenstein, E.S., Nauta, W.J.H.: A comparison of the distribution of the fornix system in the rat, guinea pig, cat, and monkey. J. comp. Neurol. 113, 337–363 (1959).

    Google Scholar 

  • Valverde, F.: Studies on the piriform lobe. Cambridge/Mass.: Harvard University Press 1965.

    Google Scholar 

  • Votaw, C.L.: Certain functional and anatomical relations of the cornu Ammonis of the macaque monkey. I. Functional relations. J. comp. Neurol. 112, 353–382 (1959).

    Google Scholar 

  • Whitlock, D.G., Nauta, W.J.H.: Subcortical projections from the temporal neocortex in Macaca mulatta. J. comp. Neurol. 106, 183–212 (1956).

    Google Scholar 

  • Winter, P., Ploog, D., Latta, J.: Vocal repertoire of the squirrel monkey (Saimiri sciureus), its analysis and significance. Exp. Brain Res. 1, 359–384 (1966).

    Google Scholar 

  • Yakovlev, P.I., Locke, S., Koskoff, D.Y., Patton, R.A.: Limbic nuclei of thalamus and connections of limbic cortex. Arch. Neurol. (Chic.) 3, 620–641 (1960).

    Google Scholar 

  • Young, M.W.: The nuclear pattern and fiber connections of the non-cortical centers of the telencephalon of the rabbit (Lepus cuniculus). J. comp. Neurol. 65, 295–401 (1936).

    Google Scholar 

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Authors and Affiliations

  1. Max-Planck-Institut für Psychiatrie, Abt. für Verhaltensforschung, München, Germany

    Uwe Jürgens & Detlev Ploog

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  1. Uwe Jürgens
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  2. Detlev Ploog
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Jürgens, U., Ploog, D. Cerebral representation of vocalization in the squirrel monkey. Exp Brain Res 10, 532–554 (1970). https://doi.org/10.1007/BF00234269

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  • DOI: https://doi.org/10.1007/BF00234269

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